Cryo-EM structure of Hepatitis C virus IRES bound to the human ribosome at 3.9-Å resolution

Nature Communications

Volumn 6, Issue , 2015, Pages

  Quade, Nick ^a   Boehringer, Daniel ^a   Leibundgut, Marc ^a   Van Den Heuvel, Joop ^b   Ban, Nenad ^a  

^a ETH ZURICH   (Switzerland)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RNA 18S; VIRUS RNA; INTERNAL RIBOSOME ENTRY SITE;

HEPATITIS; MITOCHONDRION; PATHOGEN; RESOLUTION; RNA; TRANSMISSION ELECTRON MICROSCOPY; VIRUS;

ARTICLE; BINDING SITE; CRYOELECTRON MICROSCOPY; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; RIBOSOME; RNA STRUCTURE; START CODON; GENE EXPRESSION REGULATION; GENETICS; HEPACIVIRUS; METABOLISM; MOLECULAR MODEL; PHYSIOLOGY; RNA TRANSLATION; SMALL RIBOSOMAL SUBUNIT;

EUKARYOTA; HEPATITIS C VIRUS;

BINDING SITES; CRYOELECTRON MICROSCOPY; GENE EXPRESSION REGULATION, VIRAL; HEPACIVIRUS; HUMANS; INTERNAL RIBOSOME ENTRY SITES; MODELS, MOLECULAR; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA, RIBOSOMAL, 18S;

EID: 84953860675     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8646     Document Type: Article

References (53)

1. Gravitz, L. Introduction: a smouldering public-health crisis. Nature 474, S2-S4 (2011).
2. Hinnebusch, A. G. The scanning mechanism of eukaryotic translation initiation. Annu. Rev. Biochem. 83, 779-812 (2014).
3. Kieft, J. S., Zhou, K., Jubin, R. & Doudna, J. A. Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA 7, 194-206 (2001).
4. Pestova, T. V., Shatsky, I. N., Fletcher, S. P., Jackson, R. J. & Hellen, C. U. A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev. 12, 67-83 (1998).
5. Otto, G. A. & Puglisi, J. D. The pathway of HCV IRES-mediated translation initiation. Cell 119, 369-380 (2004).
6. Brown, E. A., Zhang, H., Ping, L. H. & Lemon, S. M. Secondary structure of the 5 nontranslated regions of hepatitis C virus and pestivirus genomic RNAs. Nucleic Acids Res. 20, 5041-5045 (1992).
7. Spahn, C. M. et al. Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 291, 1959-1962 (2001).
8. Boehringer, D., Thermann, R., Ostareck-Lederer, A., Lewis, J. D. & Stark, H. Structure of the hepatitis C virus IRES bound to the human 80S ribosome: remodeling of the HCV IRES. Structure 13, 1695-1706 (2005).
9. Hashem, Y. et al. Hepatitis-C-virus-like internal ribosome entry sites displace eIF3 to gain access to the 40S subunit. Nature 503, 539-543 (2013).
10. Yamamoto, H. et al. Structure of the mammalian 80S initiation complex with initiation factor 5B on HCV-IRES RNA. Nat. Struct. Mol. Biol. 21, 721-727 (2014).
11. Locker, N., Easton, L. E. & Lukavsky, P. J. HCV and CSFV IRES domain II mediate eIF2 release during 80S ribosome assembly. EMBO J 26, 795-805 (2007).
12. Filbin, M. E., Vollmar, B. S., Shi, D., Gonen, T. & Kieft, J. S. HCV IRES manipulates the ribosome to promote the switch from translation initiation to elongation. Nat. Struct. Mol. Biol. 20, 150-158 (2013).
13. Berry, K. E., Waghray, S., Mortimer, S. A., Bai, Y. & Doudna, J. A. Crystal structure of the HCV IRES central domain reveals strategy for start-codon positioning. Structure 19, 1456-1466 (2011).
14. Lukavsky, P. J., Kim, I., Otto, G. A. & Puglisi, J. D. Structure of HCV IRES domain II determined by NMR. Nat. Struct. Biol. 10, 1033-1038 (2003).
15. Lukavsky, P. J., Otto, G. A., Lancaster, A. M., Sarnow, P. & Puglisi, J. D. Structures of two RNA domains essential for hepatitis C virus internal ribosome entry site function. Nat. Struct. Biol. 7, 1105-1110 (2000).
16. Kieft, J. S., Zhou, K., Grech, A., Jubin, R. & Doudna, J. A. Crystal structure of an RNA tertiary domain essential to HCV IRES-mediated translation initiation. Nat. Struct. Biol. 9, 370-374 (2002).
17. Rijnbrand, R., Thiviyanathan, V., Kaluarachchi, K., Lemon, S. M. & Gorenstein, D. G. Mutational and structural analysis of stem-loop IIIC of the hepatitis C virus and Gb virus B internal ribosome entry sites. J. Mol. Biol. 343, 805-817 (2004).
18. Fuchs, G. et al. Kinetic pathway of 40S ribosomal subunit recruitment to hepatitis C virus internal ribosome entry site. Proc. Natl Acad. Sci. USA 112, 319-325 (2015).
19. Voorhees, R. M., Fernandez, I. S., Scheres, S. H. & Hegde, R. S. Structure of the mammalian ribosome-Sec61 complex to 3.4A resolution. Cell 157, 1632-1643 (2014).
20. Hellen, C. U. & de Breyne, S. A distinct group of hepacivirus/pestivirus-like internal ribosomal entry sites in members of diverse picornavirus genera: evidence for modular exchange of functional noncoding RNA elements by recombination. J. Virol. 81, 5850-5863 (2007).
21. Matsuda, D. & Mauro, V. P. Base pairing between hepatitis C virus RNA and 18S rRNA is required for IRES-dependent translation initiation in vivo. Proc. Natl Acad. Sci. USA 111, 15385-15389 (2014).
22. Luttermann, C. & Meyers, G. The importance of inter- and intramolecular base pairing for translation reinitiation on a eukaryotic bicistronic mRNA. Genes Dev. 23, 331-344 (2009).
23. Psaridi, L., Georgopoulou, U., Varaklioti, A. & Mavromara, P. Mutational analysis of a conserved tetraloop in the 5 untranslated region of hepatitis C virus identifies a novel RNA element essential for the internal ribosome entry site function. FEBS Lett. 453, 49-53 (1999).
24. Easton, L. E., Locker, N. & Lukavsky, P. J. Conserved functional domains and a novel tertiary interaction near the pseudoknot drive translational activity of hepatitis C virus and hepatitis C virus-like internal ribosome entry sites. Nucleic Acids Res. 37, 5537-5549 (2009).
25. Melcher, S. E., Wilson, T. J. & Lilley, D. M. The dynamic nature of the four-way junction of the hepatitis C virus IRES. RNA 9, 809-820 (2003).
26. Hashem, Y. et al. Structure of the mammalian ribosomal 43S preinitiation complex bound to the scanning factor DHX29. Cell 153, 1108-1119 (2013).
27. Berry, K. E., Waghray, S. & Doudna, J. A. The HCV IRES pseudoknot positions the initiation codon on the 40S ribosomal subunit. RNA 16, 1559-1569 (2010).
28. Yusupov, M. M. et al. Crystal structure of the ribosome at 5.5A resolution. Science 292, 883-896 (2001).
29. Polikanov, Y. S. et al. Negamycin interferes with decoding and translocation by simultaneous interaction with rRNA and tRNA. Mol. Cell. 56, 541-550 (2014).
30. Filbin, M. E. & Kieft, J. S. HCV IRES domain IIb affects the configuration of coding RNA in the 40S subunits decoding groove. RNA 17, 1258-1273 (2011).
31. Kalliampakou, K. I., Psaridi-Linardaki, L. & Mavromara, P. Mutational analysis of the apical region of domain II of the HCV IRES. FEBS Lett. 511, 79-84 (2002).
32. Hussain, T. et al. Structural changes enable start codon recognition by the eukaryotic translation initiation complex. Cell 159, 597-607 (2014).
33. Landry, D. M., Hertz, M. I. & Thompson, S. R. RPS25 is essential for translation initiation by the Dicistroviridae and hepatitis C viral IRESs. Genes Dev. 23, 2753-2764 (2009).
34. Fernandez, I. S., Bai, X. C., Murshudov, G., Scheres, S. H. & Ramakrishnan, V. Initiation of translation by cricket paralysis virus IRES requires its translocation in the ribosome. Cell 157, 823-831 (2014).
35. Bhat, P. et al. Targeting ribosome assembly on the HCV RNA using a small RNA molecule. RNA. Biol. 9, 1110-1119 (2012).
36. Dibrov, S. M. et al. Structure of a hepatitis C virus RNA domain in complex with a translation inhibitor reveals a binding mode reminiscent of riboswitches. Proc. Natl Acad. Sci. USA 109, 5223-5228 (2012).
37. Tom, R., Bisson, L. & Durocher, Y. Culture of HEK293-EBNA1 cells for production of recombinant proteins. CSH Protoc. 2008 doi:10.1101/pdb.prot4976 (1 March 2008).
38. Blasey, H. D. & Jaeger, V. in Animal Cell Culture and Production of Biologicals. (eds Sasaki, R. & Ikura, R.) (Kluwer Academic Publisher, 1991).
39. Khatter, H. et al. Purification, characterization and crystallization of the human 80S ribosome. Nucleic Acids Res. 42, e49 (2014).
40. Tivol, W. F., Briegel, A. & Jensen, G. J. An improved cryogen for plunge freezing. Microsc. Microanal. 14, 375-379 (2008).
41. Li, X. et al. Electron counting and beam-induced motion correction enable nearatomic- resolution single-particle cryo-EM. Nat. Methods 10, 584-590 (2013).
42. Mindell, J. A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
43. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
44. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
45. Scheres, S. H. & Chen, S. Prevention of overfitting in cryo-EM structure determination. Nat. Methods 9, 853-854 (2012).
46. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
47. Jones, T. A. Interactive electron-density map interpretation: from INTER to O. Acta Crystallogr. D Biol. Crystallogr. 60, 2115-2125 (2004).
48. Pettersen, E. F. et al. UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
49. Ben-Shem, A. et al. The structure of the eukaryotic ribosome at 3.0A resolution. Science 334, 1524-1529 (2011).
50. Weisser, M., Voigts-Hoffmann, F., Rabl, J., Leibundgut, M. & Ban, N. The crystal structure of the eukaryotic 40S ribosomal subunit in complex with eIF1 and eIF1A. Nat. Struct. Mol. Biol. 20, 1015-1017 (2013).
51. Greber, B. J. et al. The complete structure of the large subunit of the mammalian mitochondrial ribosome. Nature 515, 283-286 (2014).
52. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
53. Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nat. Methods. 11, 63-65 (2014).